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Persistence of Plasmodiophora Brassicae

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Persistence of Plasmodiophora Brassicae Persistence of Plasmodiophora brassicae Influence of Non-Host Plants, Soil Fauna and Organic Material Hanna Friberg Faculty of Natural Resources and Agricultural Sciences Department of Entomology Uppsala Doctoral thesis Swedish University of Agricultural Sciences Uppsala 2005 Acta Universitatis Agriculturae Sueciae 2005: 115 ISSN 1652-6880 ISBN 91-576-6914-7 © 2005 Hanna Friberg, Uppsala Tryck: SLU Service/Repro, Uppsala 2005 Abstract Friberg, H. 2005. Persistence of Plasmodiophora brassicae - Influence of Non-Host Plants, Soil Fauna and Organic Material. Doctoral thesis. ISSN:1652-6880, ISBN:91-576-6914-7 Plasmodiophora brassicae, causal agent of clubroot disease of crucifers, has tolerant resting spores that permit its survival in the absence of a host plant. The resting spores are expected to germinate when triggered by specific substances excreted from host plant roots, but they also respond to other cues. As the zoospores emerging at germination are sensitive and short-lived, stimulation of resting spore germination is a potential method for management of clubroot disease. Certain non-host plants have been found to increase resting spore germination. The effect of four non-host plants on P. brassicae was studied in laboratory-, greenhouse- and field studies. In the laboratory, root exudate solution of Lolium perenne (Perennial ryegrass) stimulated germination of resting spores more strongly than other non-host plants tested (Allium porrum, leek; Trifolium pratense, red clover; Secale cereale, winter rye) or the host plant Brassica rapa var. pekinensis (Chinese cabbage). When grown in soil, however, no species-specific effect of any of the plants was observed on the persistence of P. brassicae. It has been claimed that resting spore germination increases in response to substances excreted from decaying plant material or to a general increase in soil biological activity. However, no change in pathogen persistence was observed when infested soil was treated with plant material or with a combination of grass material and earthworms. A bioassay made it possible to correlate disease severity with concentration of resting spores in soil. This analysis provides a coarse estimation of resting spore concentration, and smaller changes in spore load may not have been detected. Nevertheless, none of the treatments showed an influence that would render them useful in dealing with heavily P. brassicae-infested soils within short time periods. The studies emphasise the need for methods for direct and precise quantification of P. brassicae in soil. The gaps in our understanding of the life cycle of the pathogen, including the factors that determine its survival, dispersal and germination are important issues that need to be addressed before we can adequately develop management strategies to control P. brassicae. Keywords: Plasmodiophora brassicae, clubroot disease, dormancy, root exudate, germination-stimulating factor, resting spore, Lolium perenne, earthworm, soil fauna Author’s address: Hanna Friberg, Department of Entomology, SLU, SE- 750 07 UPPSALA, Sweden. Klumprotsjuka på kålväxter - inverkan av sanerande grödor, markdjur och organiskt material på Plasmodiophora brassicae Plasmodiophora brassicae orsakar klumprotsjuka på korsblommiga växter, och är ett stort problem vid odling av kålväxter. Den har tåliga vilsporer som kan överleva mycket länge i marken, något som förklarats med vilsporernas tjocka väggar i kombination med förmåga att gro bara när en värdväxt finns i närheten. De frisimmande zoosporer som frigörs då vilsporer gror är känsliga och kortlivade, och måste snabbt finna en rot att infektera. Om vilsporerna kan stimuleras att gro även i frånvaro av värdväxter ger detta möjlighet att sanera jord från P. brassicae. Förutom värdväxterna anses vissa så kallade sanerande grödor ha groningsstimulerande inverkan på P. brassicae. Effekten av sådana växter undersöktes i laboratorie-, växthus- och fältstudier. I vattenlösning stimulerade rotexudatlösning av engelskt rajgräs (Lolium perenne) vilsporerna att gro mer än övriga testade icke-värdar: höstråg (Secale cereale), purjolök (Allium porrum), och rödklöver (Trifolium pratense). Den stimulerande effekten var även större än den för värdväxten salladskål (Brassica rapa var. pekinensis). Vid odling i jord - i växthus- och fältförsök - minskade däremot ingen av växtarterna P. brassicae mer än de andra. Även ämnen som utsöndras från multnande växtmaterial och en ökad biologisk aktivitet har föreslagits minska vilsporernas överlevnad. Men i försök med tillförsel av växtmaterial med eller utan daggmasken Aporrectodea caliginosa (lermasken) märktes ingen mätbar minskning av P. brassicae. Med en biotestmetod kunde infektionen av testplantor korreleras med sporkoncentrationen i jorden. Metoden ger ett grovt mått, och det kan inte uteslutas att en eller flera av de olika behandlingarna påverkade överlevnaden i viss omfattning, men att effekterna inte tydliggörs med denna metod. För att detektera mindre skillnader krävs en mer noggrann mätmetod för P. brassicae i jord. Vi kan ändå dra slutsatsen att ingen av de undersökta behandlingarna på kort sikt kan förväntas lindra problem med klumprotsjuka i jordar med höga sporkoncentrationer. För att komma framåt i förståelsen av vilsporernas överlevnad behövs både förbättrade metoder för kvantifiering av P. brassicae och ökad kunskap om patogenens biologi. Det kan utgöra nyckeln till framtida framgångsrika metoder att bemästra klumprotsjuka. Contents Introduction, 7 Aims of the thesis, 7 Study organism: Plasmodiophora brassicae, 8 Effects of different plant species on soil microorganisms, 12 Soil fauna and plant pathogens, 12 Organic material and plant pathogens, 13 Materials and Methods, 14 Methods in analysis of P. brassicae, 14 Non-host plants, 15 Soil fauna, 15 Organic material, 16 Results and Discussion, 17 Bioassay, 17 Non-host plants, 17 Soil fauna, 18 Organic material, 19 Concluding remarks, 20 References, 21 Acknowledgements/Tack, 26 Appendix Papers I-V The present thesis is based on the following papers, which will be referred to by their Roman numerals: I. Friberg, H., Lagerlöf, J. & Rämert, B. Germination of Plasmodiophora brassicae resting spores stimulated by a non-host plant. European Journal of Plant Pathology, in press. II. Friberg, H., Lagerlöf, J., & Rämert, B. Are non-host plants useful in management of clubroot disease? (Submitted manuscript). III. Friberg, H., Lagerlöf, J., Hedlund, K. & Rämert, B. Effect of earthworms and incorporation of grass on Plasmodiophora brassicae. (Manuscript). IV. Svensson, K. & Friberg, H. Changes in microbial status as induced by earthworms and grass amendments. (Submitted manuscript). V. Friberg, H. & Hedlund, K. A bioassay method of detecting Plasmodiophora brassicae spore concentrations in soil. (Manuscript). Paper I is reproduced by kind permission of the publisher. Introduction Plasmodiophora brassicae Woron., causal agent of clubroot disease, is a severe problem in production of Brassica crops. The resting spores have the capacity to survive for at least 15 years waiting for a suitable host (Wallenhammar, 1996). This extended survival has been explained by a consequential dormancy of the resting spores. Spore germination is expected to be induced by specific substances excreted from host plant roots. It has been observed, however, that germination occurs also in the absence of host plant roots, and that it can be stimulated by various environmental factors (Macfarlane, 1970; Suzuki et al., 1992; Takahashi, 1994a, b; Begon, Harper & Townsend, 1996). The protected life of P. brassicae in the soil and inside plant roots makes it difficult to control, and fungicides do not give a complete control of P. brassicae (Karling, 1968). Despite extensive breeding programmes for resistant cultivars, the genetic variability of the pathogen has caused problems and few resistant cultivars have been produced. The pathogen has often been able to overcome the resistance after some time (Voorrips, 1995). Clubroot control today is thus restricted to cultural management methods that create an environment less beneficial for disease development, especially avoidance of all host plants, cruciferous crops as well as weeds, in the crop rotation. Although the time for a heavily infested soil to reach a spore concentration below the detection level is unacceptably long from a grower’s perspective, a sound crop rotation is the most important way to prevent severe outbreaks of clubroot disease and build-up of P. brassicae resting spores. Therefore, increased knowledge about the factors that enhance the rate of spore disappearance is highly interesting. Finding of such factors would facilitate the development of a soil management system that enables Brassica crops to be grown without reaching spore concentrations of P. brassicae that damage the crop. Aims of the thesis In this thesis, the influence of soil biological interactions on persistence of P. brassicae is investigated. Firstly, the influence of non-host plants on germination and persistence of P. brassicae was studied (Papers I &II). Secondly, the abundance of soil arthropods around infected roots compared to healthy roots and in soil without roots was investigated. Thirdly, the influence of incorporation of Lolium perenne L., alone and in combination with the earthworm Aporrectodea caliginosa Savigny, was studied (Papers III & IV). The influence of plant material was further studied in a Master’s thesis by Sillén (2003), supervised by Friberg and Rämert,
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